{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,31]],"date-time":"2026-03-31T16:16:16Z","timestamp":1774973776759,"version":"3.50.1"},"reference-count":65,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2023,5,19]],"date-time":"2023-05-19T00:00:00Z","timestamp":1684454400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Agencia Valenciana de Fomento y Garantia Agraria","award":["AGCOOP_A_2022_015"],"award-info":[{"award-number":["AGCOOP_A_2022_015"]}]},{"name":"Agencia Valenciana de Fomento y Garantia Agraria","award":["AGROALNEXT\/2022\/043"],"award-info":[{"award-number":["AGROALNEXT\/2022\/043"]}]},{"name":"Next Generation European Union and the Plan de Recuperaci\u00f3n, Transformaci\u00f3n y Resiliencia of the Spanish Government","award":["AGCOOP_A_2022_015"],"award-info":[{"award-number":["AGCOOP_A_2022_015"]}]},{"name":"Next Generation European Union and the Plan de Recuperaci\u00f3n, Transformaci\u00f3n y Resiliencia of the Spanish Government","award":["AGROALNEXT\/2022\/043"],"award-info":[{"award-number":["AGROALNEXT\/2022\/043"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>Insects have limited ability to regulate their body temperature and have thus required a range of strategies to withstand thermally stressful environments. Under unfavorable winter conditions, insects often take refuge under the soil surface to survive. Here, the mealybug insect family was selected for the study. Field experiments were performed in fruit orchards in eastern Spain. We used specifically designed floor sampling methods combined with fruit tree canopy pheromone traps. We found that in temperate climates, the large majority of the mealybugs move from the tree canopy to the roots during the winter, where they turn into belowground root-feeding herbivores to survive and continue underground the reproductive process. Within the rhizosphere, mealybugs complete at least one generation before emerging on the soil surface. The preferred area to overwinter is within 1 m in diameter around the fruit tree trunk, where more than 12,000 mealybug flying males per square meter can emerge every spring. This overwintering pattern has not previously been reported for any other group of insects showing cold avoidance behavior. These findings have implications at the winter ecology level but also at the agronomical level since treatments to control mealybug pests are, until now, only based on the fruit trees\u2019 canopy.<\/jats:p>","DOI":"10.3390\/insects14050481","type":"journal-article","created":{"date-parts":[[2023,5,19]],"date-time":"2023-05-19T10:08:55Z","timestamp":1684490935000},"page":"481","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["A Novel Insect Overwintering Strategy: The Case of Mealybugs"],"prefix":"10.3390","volume":"14","author":[{"given":"Rosa","family":"Vercher","sequence":"first","affiliation":[{"name":"Escuela T\u00e9cnica Superior de Ingenier\u00eda Agron\u00f3mica y del Medio Natural, Universitat Polit\u00e8cnica de Val\u00e8ncia, Camino de Vera, s\/n, 46022 Valencia, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sandra","family":"Gonz\u00e1lez","sequence":"additional","affiliation":[{"name":"Escuela T\u00e9cnica Superior de Ingenier\u00eda Agron\u00f3mica y del Medio Natural, Universitat Polit\u00e8cnica de Val\u00e8ncia, Camino de Vera, s\/n, 46022 Valencia, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Adri\u00e1n","family":"S\u00e1nchez-Domingo","sequence":"additional","affiliation":[{"name":"Escuela T\u00e9cnica Superior de Ingenier\u00eda Agron\u00f3mica y del Medio Natural, Universitat Polit\u00e8cnica de Val\u00e8ncia, Camino de Vera, s\/n, 46022 Valencia, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5854-1166","authenticated-orcid":false,"given":"Juan","family":"Sorribas","sequence":"additional","affiliation":[{"name":"Universitat Polit\u00e8cnica de Val\u00e8ncia, Camino de Vera, s\/n, 46022 Valencia, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,5,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Capinera, J.L. (2008). Encyclopedia of Entomology, Springer Science & Business Media.","DOI":"10.1007\/978-1-4020-6359-6"},{"key":"ref_2","first-page":"751","article-title":"Classes of insect cold hardiness","volume":"7","author":"Bale","year":"1993","journal-title":"Func. Ecol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"980","DOI":"10.1242\/jeb.037911","article-title":"Insect Overwintering in a Changing Climate","volume":"213","author":"Bale","year":"2010","journal-title":"J. Exp. Biol."},{"key":"ref_4","first-page":"421","article-title":"Importance of midfield shelterbelts for over-wintering entomofauna (Turew area, West Poland)","volume":"52","author":"Karg","year":"2004","journal-title":"Pol. J. Ecol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.1603\/EN08088","article-title":"Pupal development of Ceratitis capitata (Diptera: Tephritidae) and Diachasmimorpha longicaudata (Hymenoptera: Braconidae) at different moisture values in four soil types","volume":"39","author":"Bento","year":"2010","journal-title":"Environ. Entomol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1046\/j.1570-7458.1999.00512.x","article-title":"Reproductive status and flight activity of the overwintered Colorado potato beetle","volume":"91","author":"Ferro","year":"1999","journal-title":"Entomol. Exp. Et Appl."},{"key":"ref_7","unstructured":"Capinera, J.L. (2001). Tobacco Budworm, Heliothis virescens (Fabricius) (Insecta: Lepidoptera: Noctuidae), University of Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, EDIS."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1080\/002229300299282","article-title":"Ghost-moths of the world: A global inventory and bibliography of the Exoporia (Mnesarchaeoidea and Hepialoidea) (Lepidoptera)","volume":"34","author":"Nielsen","year":"2000","journal-title":"J. Nat. Hist."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"320","DOI":"10.2307\/3495313","article-title":"Annotated Bibliography of the Grape Root Borer (Lepidoptera: Sesiidae)","volume":"74","author":"Williams","year":"1991","journal-title":"Fla. Entomol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/0022-1910(88)90053-4","article-title":"Host-plant finding for oviposition by adult cabbage root fly, Delia radicum","volume":"34","author":"Nottingham","year":"1988","journal-title":"J. Insect Physiol."},{"key":"ref_11","unstructured":"Longo, S. (1986). Agrumicoltura, Il Recente Contributo Della Ricerca allo Sviluppo Dell\u2019Agrumicoltura Italiana, Carlo Delfino."},{"key":"ref_12","first-page":"929","article-title":"Citrus phenology as a basis to study the population dynamics of the citrus mealybug complex in Portugal","volume":"Volume 3","author":"Franco","year":"1992","journal-title":"Proceedings of the 7th International Citrus Congress"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1603\/0022-0493-94.1.291","article-title":"Seasonal movement and distribution of the grape mealybug (Homoptera: Pseudococcidae): Developing a sampling program for San Joaquin Valley vineyards","volume":"94","author":"Geiger","year":"2001","journal-title":"J. Econ. Entomol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1603\/EC09234","article-title":"Citrus mealybug (Hemiptera: Pseudococcidae) movement and population dynamics in an arbor-trained vineyard","volume":"103","author":"Cid","year":"2010","journal-title":"J. Econ. Entomol."},{"key":"ref_15","first-page":"119","article-title":"The phenology and status of Planococcus citri in the citrus groves in Israel","volume":"11","author":"Rivnay","year":"1961","journal-title":"Israel J. Agric. Res."},{"key":"ref_16","unstructured":"Klein, M. (1994). Studies of the Citrus Mealybug, Planococcus citri (Risso): Dynamics of Fruit Infestation and Biological Control. [Master\u2019s Thesis, The Hebrew University of Jerusalem, Faculty of Agriculture]."},{"key":"ref_17","unstructured":"Franco, J.C., Borges da Silva, E., and Carvalho, P.J. (2000). Cochonilhas-Algod\u00e3o (Hemiptera, Pseudococcidae) Associadas aos Citrinos em Portugal, ISA Press."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"133","DOI":"10.17660\/ActaHortic.2018.1195.22","article-title":"Monitoring and control strategies for mealybug of persimmon in Australia","volume":"1195","author":"Bignell","year":"2018","journal-title":"Acta Hortic."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1111\/j.1365-3113.2007.00408.x","article-title":"A subfamily-level classification of mealybugs (Hemiptera: Pseudococcidae) based on integrated molecular and morphological data","volume":"33","author":"Hardy","year":"2008","journal-title":"Syst. Entomol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Godfrey, K.E., Daane, K.M., Bentley, W.J., Gill, R.J., and Malakar-Kuenen, R. (2002). Mealybugs in California vineyards (Publication 21612), University of California, Agriculture & Natural Resources.","DOI":"10.3733\/ucanr.21612"},{"key":"ref_21","unstructured":"Ben-Dov, Y. (1994). A Systematic Catalogue of the Mealybugs of the World (Insecta: Homoptera: Coccoidea: Pseudococcidae, and Putoidae) with Data on Geographical Distribution, Host Plants, Biology, and Economic Importance, Intercept Ltd."},{"key":"ref_22","first-page":"9","article-title":"A review of the association of ants with mealybug wilt disease of pineapple","volume":"36","author":"Jahn","year":"2003","journal-title":"Proc. Hawaii. Entomol. Soc."},{"key":"ref_23","first-page":"185","article-title":"Studies on cotton mealybug, Phenacoccus solenopsis (Pseudococcidae: Homoptera), and its natural enemies in Punjab, Pakistan","volume":"14","author":"Arif","year":"2012","journal-title":"Int. J. Agric. Biol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1111\/j.1574-0862.2001.tb00024.x","article-title":"Economics of biological control of cassava mealybug in Africa","volume":"24","author":"Zeddies","year":"2001","journal-title":"Agric. Econ."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1080\/09670874.2020.1861363","article-title":"Crop losses and economic impact associated with papaya mealybug (Paracoccus marginatus) infestation in Kenya","volume":"69","author":"Kansiime","year":"2020","journal-title":"Int. J. Pest Manag."},{"key":"ref_26","first-page":"824","article-title":"Invasive species of mealybugs (Hemiptera: Pseudococcidae) and their threat to U.S. agriculture","volume":"104","author":"Miller","year":"2002","journal-title":"Proc. Entomol. Soc. Wash."},{"key":"ref_27","first-page":"29","article-title":"Updated list of mealybugs and putoids from Colombia (Hemiptera: Pseudococcidae and Putoidae)","volume":"9","author":"Kondo","year":"2008","journal-title":"Bolet\u00edn del Mus. de Entomol. de la Univ. del Val."},{"key":"ref_28","unstructured":"Giunchi, P., Lugaresi, C., and Pollini, A. (1988). Stato Fitosanitario della Coltura del Kaki e Difesa dalle Avversit\u00e0. II Kaki, Aggiornamenti nella Coltura. Ismea Agricoltura Ricerca, Consorcio loto di Romagna, ERSO-Cesena. Roma Ministerio dell Agricoltura e Foreste, Societ\u00e0 orticola italiana: Emilia-Romagna, Italy."},{"key":"ref_29","unstructured":"Cavalloro, R., and Martino, E.D. (1986). Integrated Pest Control in Citrus-Groves, CRC Press."},{"key":"ref_30","first-page":"38","article-title":"El cultivo del caqui en la Ribera del X\u00faquer","volume":"241","author":"Orobal","year":"2012","journal-title":"Phytoma Espa\u00f1a"},{"key":"ref_31","unstructured":"(2019, January 12). FAOSTAT (Food and Agriculture Organization Statistics Crops). Available online: http:\/\/www.fao.org\/faostat\/en\/#data\/QC."},{"key":"ref_32","first-page":"1","article-title":"Insect pests of astringent persimmon in the Western and Eastern Cape Provinces of South Africa","volume":"10","author":"Wakgari","year":"2004","journal-title":"Afr. Plant Prot."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"61","DOI":"10.3897\/zookeys.584.8065","article-title":"Three new species of mealybug (Hemiptera, Coccomorpha, Pseudococcidae) on persimmon fruit trees (Diospyros kaki) in southern Brazil","volume":"584","author":"Kaydan","year":"2016","journal-title":"ZooKeys"},{"key":"ref_34","unstructured":"Ames, G. (2023, March 02). Persimmons, Asian and American. A National Sustainable Agriculture Assistance Program (ATTRA)\u2014National Center for Appropriate Technology (NCAT). Available online: https:\/\/www.growables.org\/information\/TropicalFruit\/documents\/PersimmonATTRA.pdf."},{"key":"ref_35","first-page":"27","article-title":"Las plagas del caqui. Bases para su protecci\u00f3n integrada en Espa\u00f1a","volume":"147","year":"2004","journal-title":"Frutic. Prof."},{"key":"ref_36","unstructured":"Tena, A., P\u00e9rez, M., Catal\u00e1n, J., Juan-Blasco, M., and Urbaneja, A. (2015). El Cultivo del Caqui, IVIA. Generalitat Valenciana."},{"key":"ref_37","unstructured":"Porcuna, J.L. (2010). Gu\u00eda de Agricultura Ecol\u00f3gica el Caqui, FECOAV."},{"key":"ref_38","first-page":"52","article-title":"Especies de cotonet y su din\u00e1mica poblacional en cultivo de caqui en la Comunidad Valenciana","volume":"286","author":"Urbaneja","year":"2017","journal-title":"Phytoma-Espa\u00f1a"},{"key":"ref_39","first-page":"24","article-title":"Pseudococcus longispinus como principal especie de pseudoc\u00f3ccido en el cultivo del caqui","volume":"336","author":"Plata","year":"2022","journal-title":"Phytoma Espa\u00f1a"},{"key":"ref_40","first-page":"2684","article-title":"Seasonal distribution and movement of the invasive pest Delottococcus aberiae (Hemiptera: Pseudococcidae) within citrus tree: Implications for its integrated management","volume":"111","author":"Tena","year":"2018","journal-title":"J. Econ. Entomol."},{"key":"ref_41","first-page":"149","article-title":"Population dynamics of Planococcus citri Risso (Homoptera: Pseudococcidae) in citrus groves in Spain","volume":"26","author":"Ripolles","year":"2003","journal-title":"IOBC Wprs Bull."},{"key":"ref_42","unstructured":"(2023, March 02). MAPA (Ministerio de Agricultura, Pesca y Alimentaci\u00f3n). Available online: https:\/\/www.mapa.gob.es\/es\/estadistica\/temas\/estadisticas-agrarias\/agricultura\/superficies-producciones-anuales-cultivos\/."},{"key":"ref_43","unstructured":"G\u00f3mez-Menor, J. (1937). C\u00f3ccidos de Espa\u00f1a, Instituto de investigaciones agron\u00f3micas."},{"key":"ref_44","first-page":"37","article-title":"Las cochinillas de los agrios.: 4\u00b0 Symposium Nacional de Agroqu\u00edmicos. Sevilla 1990","volume":"297","year":"1990","journal-title":"Levante Agr\u00edcola Rev. Int. de C\u00edtricos"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1007\/BF02980445","article-title":"Management strategies of mealybug pests of citrus in Mediterranean countries","volume":"32","author":"Franco","year":"2004","journal-title":"Phytoparasitica"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1650","DOI":"10.1093\/ee\/24.6.1650","article-title":"Variegation in Coleus blumei and life history of citrus mealybug (Homoptera: Pseudococcidae)","volume":"24","author":"Yang","year":"1995","journal-title":"Environ. Entomol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1017\/S0007485311000514","article-title":"Molecular and morphological characterisation of Pseudococcidae surveyed on crops and ornamental plants in Spain","volume":"102","author":"Soto","year":"2012","journal-title":"Bull. Entomol. Res."},{"key":"ref_48","unstructured":"Beltr\u00e0, A., and Soto, A. (2012). Pseudoc\u00f3ccidos de Importancia Agr\u00edcola y Ornamental en Espa\u00f1a, Universitat Polit\u00e8cnica de Val\u00e8ncia."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1111\/j.1461-9563.2010.00501.x","article-title":"Spatio-temporal patterns and interactions with honeydew-producing Hemiptera of ants in a Mediterranean citrus orchard","volume":"13","author":"Pekas","year":"2011","journal-title":"Agric. For. Entomol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1197","DOI":"10.1111\/1365-2664.12496","article-title":"Ants as tools in sustainable agriculture","volume":"52","author":"Offenberg","year":"2015","journal-title":"J. Appl. Ecol."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Mani, M., and Shivaraju, C. (2016). Mealybugs and Their Management in Agricultural and Horticultural Crops, Springer.","DOI":"10.1007\/978-81-322-2677-2"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1017\/S0007485300038906","article-title":"Sex ratios and the status of the male in Pseudococcinae (Hem. Coccidae)","volume":"28","author":"James","year":"1937","journal-title":"Bull. Entomol. Res."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.ecolmodel.2006.03.004","article-title":"Modelling response of insect trap captures to pheromone dose","volume":"197","author":"Branco","year":"2006","journal-title":"Ecol. Model."},{"key":"ref_54","unstructured":"Balachowsky, A. (1939). Les Cochenilles de France, d\u2019Europe, du Nord de l\u2019Afrique et du Bassin Mediterraneen Reproduction D\u00e9veloppement Embryonnaire et D\u00e9veloppement Postembryonnaire, Hermann & Cie."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1002\/jez.1401460106","article-title":"Modification of the ovary of the mealybug Planococcus citri (Risso), due to aging","volume":"146","year":"1961","journal-title":"J. Exp. Zool."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1017\/S0007485311000605","article-title":"Sexual maturation and aging of adult male mealybug (Hemiptera: Pseudococcidae)","volume":"102","author":"Mendel","year":"2012","journal-title":"Bull. Entomol. Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1093\/jee\/25.4.891","article-title":"Two economic greenhouse mealybugs of Mississippi","volume":"25","author":"Myers","year":"1932","journal-title":"J. Econ. Entomol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/s12600-009-0069-9","article-title":"Can facultative parthenogenesis occur in biparental mealybug species?","volume":"38","author":"Mendel","year":"2010","journal-title":"Phytoparasitica"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1603\/AN10139","article-title":"Reproductive biology of three cosmopolitan mealybug (Hemiptera: Pseudococcidae) species, Pseudococcus longispinus, Pseudococcus viburni, and Planococcus ficus","volume":"2","author":"Waterworth","year":"2011","journal-title":"Ann. Entomol. Soc. Am."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.jtherbio.2014.02.019","article-title":"The overwintering biology of the acorn weevil, Curculio glandium in southwestern Ontario","volume":"44","author":"Udaka","year":"2014","journal-title":"J. Therm. Biol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.jtherbio.2014.07.007","article-title":"Linking energetics and overwintering in temperate insects","volume":"54","author":"Sinclair","year":"2015","journal-title":"J. Therm. Biol."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Schou, M.F., Loeschcke, V., and Kristensen, T.N. (2015). Strong Costs and Benefits of Winter Acclimatization in Drosophila melanogaster. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0130307"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.3389\/fpls.2016.01494","article-title":"Neem oil and crop protection: From now to the future","volume":"7","author":"Campos","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref_64","unstructured":"Bello, A., L\u00f3pez-P\u00e9rez, J.A., and \u00c1lvarez, A.G. (2002, January 5\u20138). Biofumigation as an alternative to methyl bromide. Proceedings of the International Conference on Alternatives to Methyl Bromide, Sevilla, Spain."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Reddy, P.P. (2012). Recent Advances in Crop Protection, Springer.","DOI":"10.1007\/978-81-322-0723-8"}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/14\/5\/481\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:38:35Z","timestamp":1760125115000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/14\/5\/481"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,19]]},"references-count":65,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["insects14050481"],"URL":"https:\/\/doi.org\/10.3390\/insects14050481","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,19]]}}}